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High Population Differentiation in the Rock-Dwelling Land Snail (Trochulus Caelatus) Endemic to the Swiss Jura Mountains

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High Population Differentiation in the Rock-Dwelling Land Snail (Trochulus Caelatus) Endemic to the Swiss Jura Mountains Conserv Genet (2010) 11:1265–1271 DOI 10.1007/s10592-009-9956-3 RESEARCH ARTICLE High population differentiation in the rock-dwelling land snail (Trochulus caelatus) endemic to the Swiss Jura Mountains Sylvain Ursenbacher Æ Caren Alvarez Æ Georg F. J. Armbruster Æ Bruno Baur Received: 9 February 2009 / Accepted: 24 June 2009 / Published online: 14 July 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Understanding patterns of genetic structure is Introduction fundamental for developing successful management pro- grammes for isolated populations of threatened species. The fragmentation of natural habitat is generally consid- Trochulus caelatus is a small terrestrial snail endemic to ered to be a major threat to many species. Population calcareous rock cliffs in the Northwestern Swiss Jura genetic theory predicts that the isolation of small popula- Mountains. Eight microsatellite loci were used to assess the tions lead to a reduction of genetic diversity. Human effect of habitat isolation on genetic population structure activities are often the main causes of habitat fragmenta- and gene flow among nine populations occurring on dis- tion, but geographical processes and/or specific habitat tinct cliffs. We found a high genetic differentiation among requirements may also contribute to natural segregation of populations (mean FST = 0.254) indicating that the popu- populations. Species with limited dispersal ability partic- lations are strongly isolated. Both allelic richness and ularly suffer from isolation, which may lead to a marked effective population size were positively correlated with genetic divergence among populations (e.g. Conner and the size of the cliffs. Our findings support the hypothesis Hartl 2004). Furthermore, in isolated populations with that T. caelatus survived on ice-free cliffs during the decreasing population size, the risk of genetic drift Pleistocene glacier advancements from the Alps. Due to the increases which may lead to a reduction of genetic diver- establishment of beech and pine forest under recent, tem- sity (e.g. Frankham 2003) and an enhanced risk of perate climate conditions, dispersal between cliffs is no inbreeding (Saccheri et al. 1998; Reed and Frankham longer possible for rock-dwelling snails such as T. caelatus. 2003). Consequently, the evaluation of the extent of iso- Our results provide basic data for developing a conserva- lation of the existing populations and their genetic diversity tion action plan for this endangered gastropod species. are of major concern to assess the risk of disappearance of any threatened taxa. Keywords Helicoidea Á Land snails Á Microsatellites Á Land snails are ideal model organisms to study popu- Population genetic structure Á Trochulus caelatus lation genetics of species with restricted dispersal ability. Several studies have focused on the micro-scaled structure of land snail populations (Schilthuizen and Lombaerts 1994; Anderson 2007; Armbruster et al. 2007a). Trochulus caelatus (formerly Trichia caelata) is a small terrestrial gastropod (shell height: 4 mm, width: 8 mm; Kerney et al. & S. Ursenbacher ( ) Á C. Alvarez Á G. F. J. Armbruster Á B. Baur 1983) endemic to the northwestern Swiss Jura Mountains. Department of Environmental Sciences, Section of Conservation Biology, University of Basel, St. Johanns-Vorstadt 10, This species is a highly specialised rock-dwelling snail 4056 Basel, Switzerland restricted to limestone cliffs between 400 and 1,280 m e-mail: [email protected] above sea level with exposed rock faces resulting in an extremely patchy distribution in a small area (Turner et al. G. F. J. Armbruster Botanisches Institut der Universita¨t Basel, Scho¨nbeinstrasse 6, 1998). Due to its particular habitat requirements and the 4056 Basel, Switzerland very limited distribution area, T. caelatus is considered as 123 1266 Conserv Genet (2010) 11:1265–1271 potentially threatened on the Red List of Switzerland may occur and whether some evolutionary significant units (Turner et al. 1994). During the last glacier advancement, (ESUs) or managements units (MUs; see Moritz 1994) can this gastropod survived in ice-free tundra regions (nunat- be determined. Our investigation will help to develop a aks) in the Swiss Jura Mountains. The temperature increase conservation action plan for this rare gastropod. during the Holocene led to the establishment of beech forest and this species had to retract to the last open areas such as rock cliffs. The present distribution of T. caelatus Material and methods coincides largely with areas that were ice-free during the last glacier advancement from the Alps (Turner et al. Field survey and sampling 1998), suggesting that this snail has not spread since the last glaciation. The surrounding forest may strongly reduce One hundred and twenty-two cliffs, spread over the entire or even prevent dispersal among distinct cliffs. Conse- distribution area of T. caelatus were examined for the quently, we can presume that gene flow (if occurring) is presence of the species between April and August 2006 restricted among populations. (Fig. 1). The cliffs examined were located at altitudes We first examined 132 cliffs in the distribution area of ranging from 380 to 1,360 m above sea level. They the species in order to determine where T. caelatus is still consist of Jurassic coral chalks. The cliff bases are cov- occurring. When sufficient numbers of individuals were ered by different stands of deciduous forests belonging to observed, samples were collected and levels of genetic Fagetum and Tilietum associations (Burnand and Hassp- variation and differentiation were investigated using acher 1999). microsatellite markers. We also conducted landscape One sampling plot (2 m high and 10 m long) was genetic analyses to determine whether population groups randomly placed along the foot of a cliff. A cliff was Fig. 1 Locations of the cliffs examined for Trochulus caelatus. Solid dots indicate cliffs where the species was found, open dots indicate cliffs where the species was not found and grey dots to populations analysed in this study 123 Conserv Genet (2010) 11:1265–1271 1267 considered as an isolated unit when it was separated observed and expected heterozygosity (HO, HE) using from neighbouring cliffs by a strip of soil ([2 m) cov- FSTAT version 2.9.3 (Goudet 1995). Heterozygote deficit ered with vegetation. In each plot, the vertical rock within populations (FIS) was estimated and divergence surface, fissures and pockets were carefully searched for from Hardy–Weinberg (HW) equilibrium was tested using T. caelatus for 10 min., and the number of individuals FSTAT with 1,000 permutations. Effective population size was recorded. The presence of other snail species (Ne) was estimated using the linkage disequilibrium (Trochulus montanus, Pyramidula rupestris, Cochlostoma method proposed by Bartley et al. (1992) implemented in septemspirale, Chondrina avenacea and Abida secale) NEESTIMATOR version 1.1.1 (Peel et al. 2004). Spearman’s was also noted. Possible associations between species rank correlations were calculated to examine relationships were tested using Chi-square tests. For each cliff the between genetic diversity (i.e. allelic richness; AR), effec- following variables were recorded: altitude (in metres tive population size and environmental parameters (cliff above sea level), the horizontal length of the cliff (with size and snail abundance). five categories: B10, 11–20, 21–50, 51–100 and [100 m), Genetic relationships within and among populations the height of the cliff (three categories: B5, 5–10 and were investigated using FSTAT to estimate F-statistics (Weir [10 m), the size of a cliff (calculated by cliff length 9 and Cockerham 1984). Isolation by distance was tested cliff height), exposure of the cliff face, number of trees using Mantel’s test (Mantel 1967) by comparing pairwise occurring at distances of 0–5 and 5–10 m from the cliff’s (FST/(1-FST)) values with the corresponding geographic foot and the cliff area (%) covered by grass and moss. distances (log-transformed) using the program FSTAT.This Relations between occurrence of T. caelatus and cliffs transformation has been showed to be more accurate in parameters were tested using Chi-square tests and logistic detecting isolation by distance than FST versus untrans- regressions. For conservation reasons, samples of ten formed geographic distance (Rousset 1997). snails were only taken in the nine largest populations. In addition, Bayesian individual assignment approach as Snail sampling was conducted on another day than the implemented in STRUCTURE version 2.2.3 (Pritchard et al. density estimate. 2000) was tested using a model of admixture with a number of populations (K) ranging from 1 to 12. Likeli- DNA extraction and microsatellite amplification hood values for ten replicates of each K value were esti- mated after 150,000 iterations (with the first 50,000 Collected snails were stored at -80°C. Genomic DNA was iterations discarded as burn-in). The best K value was extracted from the whole soft body of the snail using the chosen by applying the method of Evanno et al. (2005) DNeasy Blood & Tissue Kit (Qiagen). DNA concentration which considers a second order rate of change to determine was measured with a NanoDropÒ ND-1000 UV–Vis the most likely value of K. Spectrophotometer (Thermo Fisher Scientific) and the DNA samples were diluted to a standard concentration of 10 ng/ll. Results Eight microsatellite loci (primers 08, 09, 10, 13, 16, 18, 22 and 26) developed for T. caelatus were used (Armbr- Habitat characteristics uster et al. 2007b). PCR was performed in 25 ll volume following the protocol described by Armbruster et al. Individuals of T. caelatus were found in 24 of the 122 (2007b). Spreadex EL-400 or EL-600 gels (Elchrom Sci- (19.7%) plots examined (Fig. 1). The 24 populations were entific AG, Switzerland) were used to resolve allelic pat- situated at an altitudinal range of 460–1,360 m in an area terns by horizontal electrophoresis performed on SEA 2000 of 25 km 9 20 km. T.
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